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Journal of General Virology Journal of General Virology Polycipiviridae: a proposed new family of polycistronic picorna-like RNA viruses --Manuscript Draft-- Manuscript Number: JGV-D-17-00319R1 Full Title: Polycipiviridae: a proposed new family of polycistronic picorna-like RNA viruses Article Type: Standard Section/Category: Insect Viruses - RNA Corresponding Author: Andrew Firth University of Cambridge -, UNITED KINGDOM First Author: Ingrida Olendraite Order of Authors: Ingrida Olendraite Nina I Lukhovitskaya Sanford D Porter Steven M Valles Andrew E Firth Abstract: Solenopsis invicta virus 2 is a single-stranded positive-sense picorna-like RNA virus with an unusual genome structure. The monopartite genome of approximately 11 kb contains four open reading frames in its 5′ one third, three of which encode proteins with homology to picornavirus-like jelly-roll fold capsid proteins. These are followed by an intergenic region, and then a single long open reading frame that covers the 3′ two thirds of the genome. The polypeptide translation of this 3′ open reading frame contains motifs characteristic of picornavirus-like helicase, protease and RNA- dependent RNA polymerase domains. Inspection of public transcriptome shotgun assembly sequences revealed five related apparently nearly complete virus genomes isolated from ant species and one from a dipteran insect. By high-throughput sequencing and in silico assembly of RNA isolated from Solenopsis invicta and four other ant species, followed by targeted Sanger sequencing, we obtained nearly complete genomes for four further viruses in the group. Four further sequences were obtained from a recent large-scale invertebrate virus study. The 15 sequences are highly divergent (pairwise amino acid identities as low as 17% in the non-structural polyprotein), but possess the same overall polycistronic genome structure distinct from all other characterized picorna-like viruses. Consequently we propose the formation of a new virus family, Polycipiviridae, to classify this clade of arthropod-infecting polycistronic picorna-like viruses. We further propose that this family be divided into three genera: Chipolycivirus (2 species), Hupolycivirus (2 species), and Sopolycivirus (11 species), with members of the latter infecting ants in at least three different subfamilies. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation Response to Reviewer Click here to access/download Response to Reviewer ResponseToReviews.pdf Manuscript Including References and Figures/Table legends Click here to download Manuscript Including References (Word document) MS_Polycipiviridae_IO.docx 1 Polycipiviridae: a proposed new family of polycistronic 2 picorna-like RNA viruses 3 4 Ingrida Olendraite1,a, Nina I. Lukhovitskaya1,a, Sanford D. Porter2, Steven M. Valles2, 5 Andrew E. Firth1,b 6 7 1 Division of Virology, Department of Pathology, University of Cambridge, Cambridge 8 CB2 1QP, U.K. 9 10 2 Center for Medical, Agricultural and Veterinary Entomology, USDA-ARS, 1600 SW 11 23rd Drive, Gainesville, FL 32608, U.S.A. 12 13 a These authors contributed equally to this work 14 b Correspondence – [email protected] 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 1 33 Abstract 34 Solenopsis invicta virus 2 is a single-stranded positive-sense picorna-like RNA virus 35 with an unusual genome structure. The monopartite genome of approximately 11 kb 36 contains four open reading frames in its 5′ one third, three of which encode proteins with 37 homology to picornavirus-like jelly-roll fold capsid proteins. These are followed by an 38 intergenic region, and then a single long open reading frame that covers the 3′ two 39 thirds of the genome. The polypeptide translation of this 3′ open reading frame contains 40 motifs characteristic of picornavirus-like helicase, protease and RNA-dependent RNA 41 polymerase domains. Inspection of public transcriptome shotgun assembly sequences 42 revealed five related apparently nearly complete virus genomes isolated from ant 43 species and one from a dipteran insect. By high-throughput sequencing and in silico 44 assembly of RNA isolated from Solenopsis invicta and four other ant species, followed 45 by targeted Sanger sequencing, we obtained nearly complete genomes for four further 46 viruses in the group. Four further sequences were obtained from a recent large-scale 47 invertebrate virus study. The 15 sequences are highly divergent (pairwise amino acid 48 identities as low as 17% in the non-structural polyprotein), but possess the same overall 49 polycistronic genome structure distinct from all other characterized picorna-like viruses. 50 Consequently we propose the formation of a new virus family, Polycipiviridae, to classify 51 this clade of arthropod-infecting polycistronic picorna-like viruses. We further propose 52 that this family be divided into three genera: Chipolycivirus (2 species), Hupolycivirus (2 53 species), and Sopolycivirus (11 species), with members of the latter infecting ants in at 54 least three different subfamilies. 55 56 57 58 59 60 2 61 Introduction 62 The order Picornavirales currently comprises the families Dicistroviridae, Iflaviridae, 63 Marnaviridae, Picornaviridae and Secoviridae and the unassigned genera 64 Bacillarnavirus and Labyrnavirus. Members of the order are characterized by (i) a 65 positive-sense RNA genome, usually with a 5′ covalently linked VPg ("virus protein, 66 genome linked") and a 3′ poly(A) tail, (ii) a polyprotein gene expression strategy with 67 cleavage mainly mediated by viral protease(s), (iii) a structural protein module 68 containing three jelly-roll capsid protein domains which form small non-enveloped 69 icosahedral virions with pseudo T = 3 symmetry, and (iv) a non-structural protein 70 module containing a superfamily III helicase (or NTPase), a 3C-like chymotrypsin-like 71 protease, and a superfamily I RNA-dependent RNA polymerase (RdRp) encoded 72 sequentially in that order [1]. In contrast, families Caliciviridae and Potyviridae (for 73 example), although termed picorna-like (and informally grouped into a "picorna-like 74 superfamily") are excluded from the Picornavirales order for various reasons; for 75 example caliciviruses encode a single jelly-roll capsid protein and virions have true T = 76 3 symmetry, while potyviruses have an unrelated capsid protein, filamentous virions, 77 and encode a superfamily II instead of superfamily III helicase. 78 79 Solenopsis invicta virus 2 (SINV-2) is a positive-sense single-stranded RNA virus that 80 infects the red imported fire ant, Solenopsis invicta Buren, an invasive species in 81 southern U.S.A. [2]. Replicating virus was detected in larval and adult stages of S. 82 invicta [3]. While field infection rates are rather low for S. invicta [4, 5], there are distinct 83 fitness costs for founding queens infected with the virus [6]. Colonies established from 84 SINV-2-infected queens produced less brood and had longer claustral periods. SINV-2 85 infection was also associated with significant up-regulation of global gene expression in 86 S. invicta queens, including immune response genes [6]. The monopartite genome was 87 originally found to contain three open reading frames (ORFs) in its 5′ one third and a 88 single long ORF in its 3′ two thirds, though we show here that there are actually four 89 consecutive 5′ ORFs, one having been overlooked previously as a result of a 90 sequencing error. The polypeptide encoded by the 3′ ORF contains motifs characteristic 3 91 of a superfamily III helicase, 3C-like chymotrypsin-related protease, and a superfamily I 92 RdRp [2]. A phylogenetic analysis of RdRp sequences placed SINV-2 within the 93 "picorna-like superfamily" but outside of established virus families [7]. Isometric particles 94 with a diameter of ~33 nm were found only in ants testing positive for SINV-2 by RT- 95 PCR [2]. 96 97 By searching the NCBI transcriptome shotgun assembly (TSA) database, we identified 98 six related sequences of which five were derived from ant samples. To further explore 99 the diversity and prevalence of this group of viruses, we performed high-throughput 100 sequencing of RNA derived from Solenopsis invicta and four U.K. ant species. This led 101 to the identification of four additional viruses. During the course of this work, 1445 new 102 viruses were identified via high-throughput sequencing [8], of which four exhibit similar 103 genome organizations to SINV-2. We performed a phylogenetic and comparative 104 genomic analysis of these SINV-2-like virus sequences. All have a characteristic 105 genome organization with four consecutive 5′ proximal ORFs and one long 3′ ORF. 106 ORF1, 3 and 4 are predicted to encode jelly-roll fold capsid proteins while ORF2 107 encodes a protein of unknown function. Ant-infecting members of the group apparently 108 have an additional 5′ ORF (ORF2b) overlapping the 5′ end of ORF2 and encoding a 109 small protein containing a predicted transmembrane domain. The 3′ ORF5 encodes 110 helicase, protease and RdRp domains, is presumed to encode a VPg and potentially 111 another protein between the helicase and protease, and likely encodes one or more 112 additional proteins upstream of the helicase. The unusual genome organization and 113 phylogenetic distinctness of this group of viruses suggests they should be classified into 114 a new virus family for which we propose the name Polycipiviridae (polycistronic 115 picorna-like viruses). The characteristic complement of picornavirus-like protein 116 domains suggests that the Polycipiviridae should be included within the Picornavirales 117 order. 118 4 119 Results 120 Identification of SINV-2-like viruses 121 The SINV-2 genome was first sequenced by Valles et al. [2]. Suspicious of a large 122 apparently non-coding gap following ORF1, we resequenced the SINV-2 genome. This 123 resulted in correction of a UGA stop codon to a UGG tryptophan codon, after which it 124 became apparent that the region following ORF1 is actually occupied by an open 125 reading frame. The reannotated SINV-2 ORFs are shown in Fig.
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